A marine mystery solved (and a bit about birds)

There are a million mysteries in the Naked City of Biology, and some of them get solved. This is one of them, taken from the Japanese culture site Spoon & Tamago. It’s described in the post “The deep sea mystery circle—a love story”

Several decades ago, a Japanese “salary man” named Yoji Ookata quit his office job to pursue his real love—underwater photography. Recently, diving 80 feet down off the island of Amami Oshima (one of the Amami islands between Japan and Taiwan), Ookata saw something that nobody had ever seen before. It was a large, radially symmetrical pattern in the sand, and looked like this (note underwater camera for scale):

This and all images courtesy Yoji Ookata and NHK

The site describes this bizarre structure:

On the seabed a geometric, circular structure measuring roughly 6.5 ft in diameter had been precisely carved from sand. It consisted of multiple ridges, symmetrically jutting out from the center, and appeared to be the work of an underwater artist, carefully working with tools. For its resemblance to crop circles, Ookata dubbed his new finding a “mystery circle,” and enlisted some colleagues at NHK [a Japanese television station] to help him investigate. In a television episode that aired last week titled “The Discovery of a Century: Deep Sea Mystery Circle,” the television crew revealed their findings and the unknown artist was unmasked.

What on earth could have caused that? Was it some kind of elaborate prank, like crop circles? Not likely: this structure wouldn’t retain its integrity for long in the face of currents. But what? Try to guess before you read further.

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It’s a fish! Or, rather, a single small male pufferfish who digs the structure in the sand:

The artist at work (caption from the site)

Here it is digging:

Now why on earth would a small fish go to all this trouble to do this? (Note how elaborate the sculpture is, and how symmetrical.)

If you’re an evolutionary biologist, you might have guessed: sexual selection. A male sculpts this thing to attract females for mating. And the sculpture is decorated, too!

Underwater cameras showed that the artist was a small puffer fish who, using only his flapping fin, tirelessly worked day and night to carve the circular ridges. The unlikely artist – best known in Japan as a delicacy [JAC: perhaps this is the fugu, or edible pufferfish that has a toxic liver], albeit a potentially poisonous one – even takes small shells, cracks them, and lines the inner grooves of his sculpture as if decorating his piece. Further observation revealed that this “mysterious circle” was not just there to make the ocean floor look pretty. Attracted by the grooves and ridges, female puffer fish would find their way along the dark seabed to the male puffer fish where they would mate and lay eggs in the center of the circle. In fact, the scientists observed that the more ridges the circle contained, the more likely it was that the female would mate with the male. The little sea shells weren’t just in vain either. The observers believe that they serve as vital nutrients to the eggs as they hatch, and to the newborns.

What was fascinating was that the fish’s sculpture played another role. Through experiments back at their lab, the scientists showed that the grooves and ridges of the sculpture helped neutralize currents, protecting the eggs from being tossed around and potentially exposing them to predators.

It was a true story of love, craftsmanship and the desire to pass on descendants.

What we have here, then, is the underwater equivalent of the bowers built by Australian bowerbirds: elaborate structures to attract females (bowers, too, are often decorated, and you can see their variety among species here). One difference between the pufferfish’s structure (perhaps readers would care to name it?) and bowers is that the latter are built by birds solely to attract females, and are places where matings occur. Eggs are not laid in the bowers, but elsewhere in regular nests. The deadbeat male absconds for good after mating.

In both cases, it seems, the more elaborate the structure, and the more decorations it bears, the more attractive it is to females. We’re not sure why this is: perhaps it’s a sign to the female of the male’s vigor (indicating either good genes or the ability to dispense lots of good paternal care), or perhaps females simply have an inherent preference for more elaborate structures (I doubt this, but that was Darwin’s theory. He thought that females had an innate aesthetic sense that males evolved to cater to). Females may also have the ability to judge whether the ridges are good enough to protect their eggs.

Evidence favoring the good-genes model is that males of both bowerbirds and pufferfish don’t tend the eggs or offspring after they’re laid, so there aren’t any “direct benefits” a male able to build nice structures can give to his offspring (except making the ridges good enough to protect eggs from currents). Beyond that, males bequeath only genes. I asked my colleague Steve Pruett-Jones—an expert on the evolution of bird behavior, who also gets up early—about bowers, and he sent this answer:

Males never see the nests of females (as far as anyone knows). Despite the ‘bower’ and all of the unusual aspects of bowerbirds, the situation in bowerbirds is exactly the same as it is in birds of paradise or any other lekking species [JAC: “leks” are behaviors in which males of a species gather together in competitive displays to attract onlooking females], whether they be grouse, manakins, hummingbirds, fish, flies, etc. The question of why females should prefer males with elaborate bowers is exactly the same as why females of lekking species should prefer the males that they do. Females only get genes, nothing more. And, you know at least indirectly the literature on lekking species. There are lots and lots of correlations between aspects of male display and mating success, but very few data on the benefit to females of making the choices that they do. It is unlikely that there is only one answer, but people now generally accept the notion of good genes (as opposed to ‘no’ benefit through runaway sexual selection). Nevertheless, figuring out what those genes are and what they do for the female’s offspring remains a challenge.

There are other explanations for female preference, too, but I won’t go into them. A firm explanation for female preference still, as it does so often, eludes our grasp.

To close, here is an elaborate bower built by the male satin bowerbird, Ptilonorhynchus violaceus. Their bowers are often decorated with objects purloined from humans, and the females (ergo the males) seem to have a preference for blue. Experiments show that the females prefer to mate with males whose bowers are decorated more elaborately.

Females enter and inspect the bower before mating, and the males also perform an elaborate behavioral display as well. Here’s the artist and the consumer. Note the sexual dimorphism in color, itself an indication that sexual selection is going on here:

Here is the mating display of the male satin bowerbird. Note how the female keeps a close watch on his behavior:

And, just to show how far sexual selection can go, here’s an Attenborough piece of the masterpiece of bowers—that constructed by the Vogelkop bowerbird, Amblyornis inornata.

Sexual selection is a marvelous thing, sculpting both behavior and structures like the bower and “fish circle” (things that Dawkins would call “extended phenotypes”) throughout the animal kingdom.

55 Comments

That is just fantastic. When I have been swimming in freshwater in the US I have often seen the nests – hollows in the sand – made by bluegill sunfish. When there are lots it is pretty impressive. This work of art by the puffer fish puts them to shame. As a side note, I have also seen a bower bird nest decorated with toy soldiers! Not standing to attention, but scattered like an artful massacre around the bower.

OK, so I did guess. I thought it was some animal(s) doing something in a circle, probably involving sex.

Well, I was (sorta) right, though the animal was a lot smaller than I expected. Can’t claim much insight for the ‘sex’ bit, considering how pervasive it is in nature. Or possibly just in my overheated brain.

What I hadn’t thought was that the ‘structure’ was ‘designed’ (by the fish). That’s certainly an impressive sand cloud the little fella’s leaving behind him.

Feathers, berries, and flowers, and (I expect) the occasional bluish pebble. Plastic is a lot easier to get (at least on the east coast where this species lives), and not biodegradable, so modern Satin bowers are a lot busier and bluer than their ancestors.

The males, after getting adult plumage and starting a bower at the age of seven or so, spend a large proportion of their time stealing from each other, so it’s just like economics.

Other bowerbirds have different colour preferences; e.g. Greats and Westerns like white and pale green, and in their bowers you see feathers, berries, flowers, quartz pebbles, and bones.

I guessed the structure was produced by jet action from the centre point. Either jetting vertically downwards with variable force or horizontally outwards whilst rotating. Amazed to find such a fish could use its tail fin as a power tool! Wikipedia says the puffer fish uses its tail as a defense mechanism to get out of jaws quickly by producing a sudden power burst. Somebody needs to get that amazing picture up!http://en.wikipedia.org/wiki/Tetraodontidae

I would imagine complex behaviors such as this require complex neural wiring. So a male that does a good job must have sturdy genes.
A few questions for JAC if you dont mind:

Do the males that win these competitions have a lower parasite load? Are there any objective measures to show they’re healthier than the losers?
Are the genus’ of animals that engage in these behavior more species rich? In other words does it pay for a species to be this picky?
Do these species have fewer recessive lethals?

I’m not sure about leks, but in some bird species males with more parasites become less colorful, more scruffy looking, and win fewer mates. In my book (with Allen Orr) on Speciation, we show evidence that groups more prone to sexual selection do seem to produce more species, though the evidence is not strong. I don’t know bupkes about recessive lethals in any birds, and I don’t think anyone else does, either.

Don’t know anything about the recessive lethal question either, but indeed, in at least a few lekking species, successful males have fewer parasites. That’s also true of some other birds and an assortment of other species as well. It’s not just that the parasite or pathogen makes their feathers seem scruffy, it’s that parasite resistance is potentially a driver of female choice via genetic interactions between host and pathogen. Or at least it is if you buy a hypothesis that Bill Hamilton and I proposed a while back.

The precision is really amazing. Most humans, with our massive brains and hands, could not create that with such precision without resorting to layout tools. And yet every male of this little pea brained fish species does it regularly.

Behaviors like this really illustrate, for me, how powerfully capable the process of evolution is of creating (resulting in?) such incredible complexity. And, also, how contingent it is.

Why did this species evolve this particular behavior as a means of attracting mates and protecting eggs? That is just what happened. No planning, no magic, but even more amazing.

“Are you suggesting that the fish’s aesthetic sense plays no role in the quality of that design?

Commenting on the fish’s aesthetic sense was not in my thoughts at all, so no. I was not intending to suggest anything like that. I definitely agree, that is an interesting question. I think any discussion would first have to define aesthetic sense clearly for this context.

By contingent I meant “uncertain, subject to chance.” And that was regarding evolution in general, not this particular phenomenon.

“You’re definitely wrong about the first point you make. You’re probably one of those humans who doesn’t work with his hands.

I do “work with my hands”, fairly well compared to average. Which probably contributes to my opinion that most people could not create that shape with the level of precision the fish does without using tools. I did not mean to say that no people can, and I did not mean to say that the average person could not be trained to do so. I am aware that there are people who can create precise shapes free hand, but that is not the norm. Not even among artists, of which I have a good bit of experience working with. By that I mean a large percentage of artists are not very good “working with their hands” either, and rely on “concept” being deemed of greater aesthetic value.

“I forgot my reference at home so I did this Futura-based logo from memory:”

Interesting that we come to different conclusions from the same experience. Getting good at calligraphy had me thinking anyone could do this if they also worked hard at it, though admittedly a bit of talent / physical and mental capacity helps.

The way you worded your response to my question about the fish’s aesthetic sense has me hoping you could shed some light on something that’s been bugging me for some time. It’s actually one of the reasons I read this “blog”:-

I can’t wholeheartedly and wholly accept the contingent nature of evolution precisely because of stuff like this. When I look at bower birds and how some animals select their mates, and when I consider how I selected my own mate I can’t help thinking that there is more to it than chance. That is, I can’t help thinking that animals themselves, to some extent, through the way they choose their mates, actually drive their own evolution. I’m not suggesting that we have evolutionary advantage in mind when we choose our mates, but certainly aesthetic sense plays a role (for current purposes, I’d define it crudely as what animals like and don’t like). My wife’s incredible brain was a major attraction to me when I met her and I pursued her very much for that quality so it is not entirely a matter of chance that we now have a son who today came home from his first marimba / vibraphone lesson and the first thing he did was write a rather lovely little composition for it and play it to us.

Of course, most living things, don’t do any selection of mates but a lot of birds and animals even fish clearly do, so I have difficulty seeing how, their case it can be characterised as just “natural selection.”

Selecting a mate is not any different in principle than bees selecting which flowers to collect nectar from, or birds selecting which insects to eat. The selective landscape in which organisms compete necessarily includes the actions of other organisms, including potential mates as well as potential predators or prey. So it’s all natural selection, which (as I see it) includes sexual selection as a subset.

Evolution is, emphatically, not just chance. Chance is one aspect, but Natural Selection is not a random phenomenon. It is like a filter that only passes those changes to an organism that result in that organism surviving to reproduce. This is just the opposite of chance.

The concept of contingency in biology is that an organism’s evolution is constrained by historical events that are often random. What I had in mind when I commented above is that of all the possible ways for attracting a mate that evolution could have resulted in for this little puffer fish, its evolutionary history resulted in this particular spectacular behavior.

“Aesthetically” pleasing body forms and behaviors are like markers that correlate with fitness. It just happens to be true that that is the case. In general terms, not necessarily the case in every individual, a more symmetrical, colorful, more intricate, what have you, an organism’s physical appearance and or behavior is, is in fact an accurate indicator of fitness. The behavior of selecting mates that have these markers is a trait that has been successful at passing through the filter of Natural Selection. It certainly seems possible that an organism’s “aesthetic sense” has evolved because it is useful in selecting fit mates.

“That is, I can’t help thinking that animals themselves, to some extent, through the way they choose their mates, actually drive their own evolution.”

In a very real sense that is true. I don’t think (could of course be wrong) that many evolutionary biologist’s would have a problem with that idea. But, the organism need not, and in most cases is not, aware of what is going on. And the choosing behavior is itself a product of the organism’s evolutionary history. An organism does not consciously guide or modify its evolution, though present company may soon be excepted. Everything about an organism, including its behavior, is a product of evolution.

I was thinking it was some critter, somewhat like an uber sand dollar or a star fish, making that artful sand mandala, but a little puffer fish?! Wow.

The bower bird is one of my favourite critters. I remember seeing videos of male house-building behaviour, where a male bird will even steal from another competitor’s stash or even trash his “ardour arbour”.

I can only speculate that females go for this stuff because the males have gone to all that trouble and thus displayed mental and physical prowess and therefore good genes. It’s a tough game out there, the mating game, and the first thing to do is to catch the female’s eye. 😉

Actually, I’d like to propose calling it a “Zoid”, in honor of the eminent Dr. Zoidberg, whose species (the Decapodians) build similar mounds on the beaches of Decapod 10, with apparently similar purpose.

These are the impress ons left by jebus wheels which are brot fourth in the bible the fish has been endowed by god with the bility to make a long flat excatvation into which the female is to deposit its eggs the fish can cents that it hasnt not been successful in making a long flat excatvation so continue with farther attempt and in that way the impress ons left by the jebus wheel is exposed the jebus wheel itself is sent down to heaven as soon after the accident (wheels flying off the jeebus) as hour(YOUR) christian gods can get to it. There is but one god and they are the gods of the christians you will go to hell and burn forever without acceptance of HIM or magical garments under.

My brother, hast though not read in the book of Ezekiel where it says, “As I looked at the living creatures, I saw a wheel on the ground beside each creature with its four faces. This was the appearance and structure of the wheels: They sparkled like chrysolite, and all four looked alike. Each appeared to be made like a wheel intersecting a wheel. As they moved, they would go in any one of the four directions the creatures faced; the wheels did not turn about as the creatures went. their rims were high and awesome, and all four rims were full of eyes all around.”
Clearly this shows that thou speakest heresy.

I don’t know- when I think about humans who dedicate considerable time and energy to producing artworks (painters, musicians, poets, actors, etc.), I think of people who have an abnormally larger number of marriages per capita. So the marriage rate might well increase!

🙂 I don’t think that’s the problem. The real problem is once the eggs are laid all the tasteful, artful courtship activity ceases and marriage becomes a less attractive-looking option to the unmarried lot.

Fascinating post! Perhaps I’m just in a pedantic mood, but I think this statement shouldn’t be made, even if negated/clarified afterwards.

“What we have here, then, is the underwater equivalent of the bowers built by Australian bowerbirds: elaborate structures to attract females”

The fact these structures contain eggs, are likely to confer survival benefits to offspring, and can thus be directly evaluated as a resource by the female…is the precise reason that these aren’t the equivalent of bowers. I think the overlap in beauty is distracting us from the fundamental differences.

I see no evidence puffer fish build this sophisticated, large underwater mound off the coast of Japan other than a photo of the species burrowing in sand. Until we see the published scientific paper from a behavioural aquatic ecologist documenting how such a sophisticated mound was built by this fish the jury is defintely out. I am not a puffer specialist, but it is my understanding such sophisticated, mind boggling behaviour has never been observed before in thousands of years of human observation. Show me the evidence, a complete in situ video, or any other evidence the puffer is capable of this. By the way, Darwin’s grand 19th century theory is as dated as marxism and freud. Please. Read Thomas Nagel’s Mind and Cosmos, David Berlinski’s The Devil’s Delusion, Michael Behe’s Darwin’s Black Box, and Rupert Sheldrake’s Science Set Free. Show me the evidence.

[…] to create these symmetrical constructions almost a couple of meters in diameter! What for? Well, as Jerry Coyne put it, “if you’re an evolutionary biologist, you might have guessed: sexual selection. A male sculpts […]